Low conservation of gene content in the Drosophila Y chromosome

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Abstract

Chromosomal organization is sufficiently evolutionarily stable that large syntenic blocks of genes can be recognized even between species as distantly related as mammals and puffer fish (450 million years (Myr) of divergence)1,2,3,4,5,6,7. In Diptera, the gene content of the X chromosome and the autosomes is well conserved: in Drosophila more than 95% of the genes have remained on the same chromosome arm in the 12 sequenced species (63 Myr of divergence, traversing 400 Myr of evolution)2,4,6, and the same linkage groups are clearly recognizable in mosquito genomes (260 Myr of divergence)3,5,7. Here we investigate the conservation of Y-linked gene content among the 12 sequenced Drosophila species. We found that only a quarter of the Drosophila melanogaster Y-linked genes (3 out of 12) are Y-linked in all sequenced species, and that most of them (7 out of 12) were acquired less than 63 Myr ago. Hence, whereas the organization of other Drosophila chromosomes traces back to the common ancestor with mosquitoes, the gene content of the D. melanogaster Y chromosome is much younger. Gene losses are known to have an important role in the evolution of Y chromosomes8,9,10, and we indeed found two such cases. However, the rate of gene gain in the Drosophila Y chromosomes investigated is 10.9 times higher than the rate of gene loss (95% confidence interval: 2.3–52.5), indicating a clear tendency of the Y chromosomes to increase in gene content. In contrast with the mammalian Y chromosome, gene gains have a prominent role in the evolution of the Drosophila Y chromosome.

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Figure 1: Synteny analysis of the kl-5 gene.
Figure 2: Gene movements in the Drosophila Y chromosome.
Figure 3: Posterior density of the net rate of Y-linked gene gain in the Drosophila phylogeny.

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Acknowledgements

We thank S. Kumar, P. O’Grady, T. Markow, A. J. Bhutkar, S. C. Vaz, E. Betran, A. A. Peixoto, P. H. Krieger and P. Paiva for comments on the manuscript and/or for sharing their unpublished results. We also thank T. Pinhão, A. Bastos and F. Krsticevic for help with the experiments, K. Krishnamoorthy for statistical advice and M. Fetchko for help with GenBank submission. This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq, Coordenação de Aperfeiçoamento do Pessoal de Ensino Superior-CAPES, FAPERJ, FIC-NIH grant TW007604-02 (A.B.C.) and NIH grant GM64590 (A.G.C.).

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Correspondence to Antonio Bernardo Carvalho.

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Supplementary Information

This file contains Supplementary Discussions, Supplementary Methods, Supplementary Figures 1-11 with Legends, Supplementary Tables 1-5, Supplementary References and Supplementary Notes. (PDF 2733 kb)

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Koerich, L., Wang, X., Clark, A. et al. Low conservation of gene content in the Drosophila Y chromosome. Nature 456, 949–951 (2008) doi:10.1038/nature07463

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